EC #19-B - The Chemistry of The Sulfur Cycle And Habitat Change

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EC #19-B - The Chemistry of The Sulfur Cycle And Habitat Change
Bacteria and Nitrogen Cycles
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Tim Visel, The Sound School
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July 2020
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October 29, 2020  Environment Conservation Thread
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A Note from Tim Visel

When I started these nitrogen and bacteria newsletters in 2014 (What About Sapropel and the Conowingo Dam, 9/29/14) it had only been a few years since EPA released an updated Long Island Sound nitrogen model.  I tried to get natural bacteria generated nitrogen counted (included) as it could swing from nitrate in cold to ammonia in heat.  Not including bacteria nitrogen in effect missed both nitrate in cold and in heat bacterial ammonia surges.  The population of each bacteria gave mother nature "a free pass" for that nitrogen.  In cold the bacteria that release nitrate (bacteria) is largely decided by heat and oxygen – less oxygen and bacteria that use sulfate as an oxygen source now produce sulfides – as mentioned many times in the historical fisheries literature as the "smell of rotten eggs."  These cycles of nitrogen were connected to climate cycles.

Most of my concern about the Long Island Sound nitrogen model is that it ignored the buildup of organic matter (sapropel) and the sulfides from it, and the ability of "new" sapropels to purge ammonia important to HAB blooms.  The sulfur/sapropel cycle was important to the nitrogen cycle, as it enhances a ever present bacterial "war" between bacteria and the nitrogen cycle itself, who literally gets to eat what organic matter and how this in turns generates more algal plant tissue, impacting those who need prefer nitrate and those (such as brown tides) who prefer ammonia.

Farmers are not surprised by this, their bacteria battle is well known in the soils that produce crops.  It is also known that extreme heat and drought can dramatically change soil chemistry for farmers but sulfate is usually limiting and farm soils are in contact with atmospheric oxygen.  That changed in the 1970's, drought and hot temperatures greatly alarmed Europe and its foresters overseas.  This was to be called the "forest dieoff" – or Waldsterben controversy that blamed human pollution but was largely from the climate cycle of soil sulfide and to a much lesser degree "cultural" human pollution.  At the time it was though that in a generation the German forests would be all dead – but that did not happen.  Instead the prolonged heat would in time be linked to increased diseases and pathogens (much larger issues) that feasted upon the dead and weakened trees.  It was just not one factor to the forest dieback but related to several seemingly at the time unconnected but, in fact, they were, heat, drought, soil sulfide formation, tree and canopy yellowing, disease and then die off.  When the rains and cooler temperatures returned to German forests they then recovered. 

In the end changes in trees species from fires and clear cutting had more lasting impacts upon German forests, its forest soils, from the elimination of beneficial soil bacteria rather than just pollution.  This sulfide toxicity is also a factor in other plant die-offs, such as eelgrass and salt marsh plants.  I do see efforts to include the sulfur cycle in recent marine studies as similar sulfide die offs occur here as well. 

In subtidal soils in estuarine waters the largest source of sulfur perhaps, is not man, but nature – dissolved sulfate.  Indications are so that EPA will acknowledge the importance of sapropel marine compost (bacteria) ammonia as it now encourages farmers to produce the same compost substance under another term "anaerobic digestate" or "AD."  This is accomplished by heating liquid manure and sealing it from oxygen, for anoxic "bacterial digestion" much the same process in natural sapropel formation in shallow waters in long periods of heat with low oxygen levels.

This in effect is a manmade sapropel –whose definition is putrefaction of organic matter without oxygen.  A recent term of anaerobic digestate is often used.  Anaerobic digestion from waste is promoted as a way to control (and possibly reuse methane gas) as the by-product of composting bacteria.  This compost is often heated to speed bacterial actions hydrolysis, acidogenesis, acetogenesis and methanogenesis.  Although we continue to focus upon analytical measures of pollution a bias from pollution control from "point source" discharges – a "pipe," human caused, we continue to fail to include biological generations of sulfide (or nitrogen) from natural anaerobic compost.  It appears because it cannot be perhaps directly connected to human inputs and therefore not a "new" pollution substance.  In either case large amounts of natural ammonia pollution was not counted.  A publication titled "Nitrogen Inputs to Seventy–Four Southern New England Estuaries – Application of a Watershed Nitrogen Loading Model," Latimer and Charpentier, Estuarine Coastal and Shelf Science (2009) pg. 129 – mentions bacterial nitrogen release as internal nitrogen regeneration – and not included directly in nitrogen model formation – and contains this statement:

"The sediment has been described by others to be a net sink, except during summer periods where it may source (Hawes et al, 2003); in either case it is not "new" nitrogen. Therefore, it was not included."

The ability of bacteria to release large amounts of ammonia from sealed composts was long known to the farm community.  They called it harbor mud and spread it on coastal fields for centuries here, even in Connecticut.  This process could be termed the harvest of natural anaerobic digestate compost.  This marine compost was spread upon farm fields to replenish depleted organic matter. 

The same anaerobic composting reactions occur in lakes and reservoirs that trap compost organics.  In heat these reservoirs themselves can become huge anaerobic digestors as bacteria decompose the compost, releasing ammonia and methane gas into the atmosphere.  But this process releases a high amount of ammonia as well, (the opposite occurs in compost with oxygen – nitrate is dominant and why garden composters turn over composts to introduce more oxygen into them) into shallow bays and coves.  High ammonia can reduce the production of methane and increase C02 from this compost.   This is the case study for the Conowingo Dam as here tens of feet of compost has collected that perhaps sheds enormous amounts of ammonia.  Natural gas primarily methane is frequently contaminated from hydrogen sulfides (H2S) from bacteria sulfate sulfur processes.   
   
The gas is often cleaned before it can be used from A. D. digestors without producing sulfuric acid. The compost itself (digestate) occurs deep in trapped deposits such as these behind the Conowingo Dam and the release of storm rainfall "digestate" to Chesapeake Bay.  The presence and formation of sapropel in reservoirs system out west has been identified as a significant problem for lakes with a strong thermocline – a sharp temperature boundary and oxygen depletion behind dams.  This account is from the 2017 Annual Water Quality Report – Central Arizona Project CAP and Arizona State University, Phoenix, AZ and describes the problem of sapropel:

"Lake Pleasant depth profiles indicate that thermal stratification occurred in the summer months.  The upper layer (epilimion) was oxygen-rich with a higher temperature, as well as having a slightly higher pH.  The lower layer (hypolimion) was lower in dissolved oxygen with lower temperatures and slightly lower pH.
The oxygen deficit conditions at the lower depths may cause sediment nutrient release through the process of reduction.  If the sediment/water interface is exposed to prolonged periods of anoxia, reducing conditions allow the formation of nutrients previously unavailable for organisms.  Reduction of these nutrients causes taste and odor changes in the water.  This reduction may lead to sapropel formation, a compound that is high in hydrogen sulfide and methane and has a shiny black color due to the presence of ferrous sulfide.  This compound is responsible for the occasional "rotten egg" odor associated with releases from the hypolimion layer through the lower portal on the intake towers.

Nutrients, such as nitrogen and phosphorous, become unbound from their ionic association with metals, such as iron, and manganese.  This process may free up nutrients, which contribute to algal blooms in the canal system.  Precipitates of iron and manganese cause discolored water and treatment problems."   
This process also occurs in low oxygen hot sea water habitats. Sulfate in sea water is a huge source of oxygen for bacteria in the marine environment – they just need the food as well, the organic matter of both land and sea. These composts can collect downstream of dams and form marshes in low energy areas.  Often these marshes are "new" and exist above previous bottoms.

In heat, the sulfate reducing bacteria thrive after heavy rains but instead of nitrate it is now releasing ammonia.  In small bodies of water, the bacterial release of ammonia is a huge concern and feeds plants that can use it such as "HABS" adding organic matter to feed more sulfate reducing bacteria. If a bay or cove has restricted flushing this ammonia (bacterial) can slosh back and forth during tidal cycles for days building to higher levels that can support immense blooms of plants that need ammonia or thick growths of other plants (macroalgae) that cover submerged grasses. These in turn die and support more sulfate reducing bacteria – that in turn waste additional sulfides as a metabolic process, as sulfides levels increase as well the rotten egg smell. This happens in high heat and low energy. That is why dead bottoms grow larger in late summer and smaller in winter.  It is also the reason the negative impacts of "black water" are more noticeable in warm to hot periods with little storm energy. We often can smell the sulfides. This impact was mentioned in a New York Times article titled "Growing at Europe's Subsidized Farms, Pollution, New York Times, pg. 1 Thursday, December 26, 2019 by Matt Apuzzo, Selam Gebrekidan, Agustin Armendariz and Jin Wu. The article talks about dead zones in the Baltic Sea – linked to farm runoff pollution.  The article mentions the sulfur cycle as we do here by the smell of rotten eggs but fails to include sulfate bacterial actions that produce the sulfides. This quote could be from any US Estuary after prolonged heat and little energy or vertical mixing – pg. A9 has this portion:

"One morning in November, Daniel Rak, a seasick oceanographer, watched as his colleagues on the research shop Oceania lowered cameras and a sensor to the floor of the Baltic Sea. When the instruments resurfaced, Mr. Rak ducked into an onboard laboratory and confirmed his suspicions, the seafloor did not have enough oxygen to support life. His ship was in a dead zone. The cameras revealed a barren landscape. There were no worms, no clams and no mollusks. "They all need oxygen, and they are gone" he said. The only signs of life were colonies of luminous bacteria that thrives without oxygen. A scoop of dirt from the sea floor smelled "like a thousand rotten eggs."

While the article highlights the impact of low oxygen it does not address how the soil got the hydrogen sulfide smell?  If the temperature becomes extremely hot -these high sulfide locations may start a sulfide event, an underwater sulfur "fire" which grows as more fish, shellfish and plants die – providing more fuel for greater sulfide production.  The dead zone grows in size like a forest fire consuming oxygen requiring life before it.
The die offs of salt marsh, eelgrass, forests, grass and fish and shellfish kills all have a bacterial sulfide connection. While many articles may mention the smell of rotten eggs regarding these die offs (often with sensational photos) very few articles mention the source of the sulfides, or the presence of sulfate reducing bacteria.

For instance, many studies link high nitrate levels in coastal waters from farm soils but that is natural, low height crops grass and grains often fail to atomize rain drops before striking the ground (as compared to forest soils).  This rain energy pounds the ground and releases minute soil particles that contain nitrogen compounds.  Once land is cleared for crops, the movement of water containing nitrogen compounds is a natural result.  The way nitrate is made into an ion and passes in water or into root tissue is by soil bacteria.  Farmers add organic matter (composts) into soils to feed the bacteria that enable plants to access nitrate ions and other plant nutrients – without bacteria these soils become less "fertile" and crop production from them declines.  This is an organic depleted soil often termed a "dying soil." This is how natural conditions and manmade actions interact.  It is natural for nitrate to move from cleared soils as it is for storm water flows to increase from paved surfaces.  Farmers long noticed this movement of soil particles with nitrogen and planted cover crops such as winter rye.  (I would do this for our large family garden growing up purchasing rye seed at Clinton Grain Co). 

Since society as a whole realizes that value and significance of agricultural soils while at the same time often criticizing the impacts of such organized food production?  Floods and droughts are beyond the control of farmers yet the need of food continues to increase.  The same conflict has happened in our fisheries, the seafood has appreciated in cycles of abundances but criticized when these same populations decline – the aspect of overfishing when in fact it is often natural cycles (See the 2018 NOAA report on The NAO released Marine Fisheries Review by Clyde L. MacKenzie, Jr. and Mitchell Tarnowski).

The impact of natural cycles in seafood abundance is just being discussed today.  We also have cycles of compost sulfides.  That is why in 2014 articles about the Conowingo Dam, first attracted my attention here we have a manmade compost pile (since the Dam construction date provides a critical "time stamp") a collection of millions of tons of bark, grass cuttings, farm and field waste, blossoms, nuts, twigs and leaves collected and rotting behind a flow constriction – the dam.  Here we are able to perhaps measure what low or no oxygen composting means to our inshore fisheries, oysters, blue crabs and striped bass.  It is known that a century ago marine mud when sealed in a barrel purged ammonia – absent of oxygen.  This bacterial process has purged tremendous amounts of ammonia into shallow waters.  When heavy deposits of organic matter moved downstream (as from heavy rains after tropical systems) the sulfide formation and periodic sulfuric acid release could impact shallow water habitats for a generation.  (Imagine someone overnight dumping 8 feet of compost on a lawn).  The Conowingo Dam articles in 2014 reflected upon the fact that the top of the compost pile had reached almost to the dam top.  Heavy rains now just moved this compost downstream.  While this has an impact, by burying oyster and clam habitats the chemical reduction of organic matter sealed from oxygen and then re oxidized could have even more profound long term habitat changes.  (Recent studies in Florida's Indian River lagoon identified "black mayonnaise" as a significant source of ammonia).  Understanding subtidal soil chemistry is key to understanding estuarine habitat quality and then its fisheries – my view, Tim Visel. 

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Blue crab as an indicator species -

When in 2012 large numbers of yellow face blue crabs showed up here in waves in Long Island Sound they were extremely hard shells had a band of yellow around their mouth or were darker brown or rusty splotches. Those stains are now thought to be the result of over wintering in low salinity areas (nearly all of the yellow face crabs were male) that obtain tannins from their river deposits, particularly from the Housatonic River.  Waters flowing from peat or organic deposits often leave a yellow or brown stain or household appliances. It is now thought these substances interact with the shell and leave the same characteristic yellow stain.  Several crabbers from down south called these "river crabs" and I believe they were correct – they had hibernated in our rivers – those that obtain large amounts of leaves and crabs the subject to tannins. The oak leaf is known to contain yellow pigments and yellow brown stains are frequently mentioned drinking water quality reports as from peat or marsh waters also in conjunction with hydrogen sulfide smells.  Entire product lines exist to remove these yellow stains from household fixtures.  This is usually attributed to water with high levels of sulfide.

To fully examine the role of sulfides, and bacterial reduction of organic matter in low oxygen conditions and its impact upon shore life a review of salt marshes is a help.  Here over hundreds of not thousands of years terrestrial organic deposits formed in low energy areas and in time broke the seawater surface.  This was no easy feat at times overcoming both land subsistence and sea level rise and is attributed to the rise of forests and the collection of loose unconsolidated terrestrial matter (also termed Duff) or leaves from the beginning of forest soils.  With the ability to examine tannin "signatures" or organic blueprints we can determine what was the dominant organic matter constituent.  To hold and bind organic matter and keep it in place would take underwater vegetation – such as eelgrass and terrestrial grasses that could hold them once they became tidal – Spartina or cord grass.  That is the salt meadow plant monocultures we can see today on many salt marshes.  But what are salt marshes – just sapropel/peat that has reached the air and with it oxygen.  It is subject to the same decomposition processes as below the water and we can see these processes in high peat organisms that have adapted to this, at times a harsh habitat – such as plants. 

Oxygen levels on the surface of salt marshes are higher and bacterial decomposition is faster than the much slower (Sulfur bacteria) than oxygen deficit sulfur reduction process below (it could be said that difference helps the marsh develop) we can see what happens to this battle between oxygen and sulfur in the compounds that accumulate or purge from them.  The surface oxidation of organic matter is much different, much quicker releasing nitrogen compounds as any backyard compost.  Below the peat surface is quite another matter.  Here exists a type of conflict or battle between bacteria that reduce organic matter using sulfur compounds particularly sulfate which is naturally abundant in sea water.  Here nitrogen and phosphate collects as it is stored (and what made it a fertilizer a century ago).  Spartina (cord grass) is a vegetation crust on a stabilized sapropel deposit that prefers the oxygen environment on the peat surface.  Because of the extremes of climate, the heat of summer and cold of winter Spartina has the ability to resist sulfide toxicity and the negative impacts of sulfate digestion with sulfuric acid.  Similar to subtidal deposits any mechanical disturbance (by crabs) helps deliver oxygen into the marsh surface below.  Fiddler crab burrows for example aerate surface layers and anyone will recognize the Swiss cheese look of burrows along marsh banks or channels.  Although not what we usually consider cultivation of terrestrial soil – it is an activity that accomplishes much the same result – as any mechanical disturbance of the marsh sediment interface – much as bioturbation described above.  Terrestrial composters measure soil health by the number and diversity of microorganisms found in it.  ("Sow bugs" that live in terrestrial compost deposits are actually crustaceans and related to lobsters and the blue crab.) The more oxygen is mixed in the more favorable the result for compost diversity.

In a book titled "The World of the Salt Marsh by Charles Seabrook (2013, he mentions the role of cultivators – burrowing organisms that can live in high organic deposits and help reduce sulfides.
And the species that appears to do the most aerating in Spartina and eelgrass meadows are crabs.  The crab species, especially fiddlers for Spartina and green crabs for eelgrass appear to have large roles in cultivating sapropel above and below the waterline (It is important to note that in the 1960's and 1970's lobsters would also often burrow into this habitat in a structure limited region – western Long Island Sound.  This was during a negative NAO – and was colder and allowed it is thought oxygen levels to be higher and likely kept toxic sulfides below lethal levels – as the NAO turned positive gradual warming occurred from 1972 to 2012 and in the late 1990s these burrowed out chambers often became deadly from suspected sulfides).

Both fiddler crabs and purple marsh crabs burrow or dig into these substrates and allow oxygen into this organic matter.  Seabrook (2013) states that such activity (salt marsh) reduces toxic sulfide accumulations in the marsh and also references studies that fiddler crabs were excluded in marsh study plots – the growth height of Spartina decreased.  Bertness (1985) reported that "crab burrows were showing to increase soil drainage soil oxidation – reduction potential and the in situ decomposition of below ground plant debris" (Fiddler Crab Regulation of Spartina alterniflora Production on a New England Salt Marsh – Ecology, 1985).
Both Spartina and eelgrass have unique biological features that allows them to live in these high sulfide subtidal environments – up to a point.  A quick review points to why salt hay (cord grass) and eelgrass were once very valuable resources.  Salt hay did not break down quickly and when it did, it released nutrient salts.  Eelgrass was a valuable insulation product because it did not burn from high silicon leaf levels.  Salt hay production increased when meadow peat was drained exposing more of the peat to oxygen.  This in turn now favored bacterial nitrate – a nitrogen compound plants needed such as salt hay species.  Salt hay then grew thick and lush with this nitrate source now close to its roots.
Both plants eelgrass and spartina have specialized root tissue that enables it to move oxygen to its most sensitive root tissue – again up to a point.  In very high sulfide levels both Spartina and eelgrass die off.  This sulfide-sulfuric acid environment is largely governed by heat and what types of bacteria feed upon the organic matter in which these plants live, the sulfur reducing species separated from oxygen by the depth of the organic deposit itself.

These two plants therefore developed habitat "defensive" attributes which help them overcome these habitats and points to coping with sulfide production by its oxidation.  Stumm and Morgan (1970) Aquatic Chemistry termed sulfide oxidation is one of the most often naturally occurring reactions, and at least some amount of sulfuric acid is always released – this highly corrosive substance directly attacks silicate structures leading to both internal and external degradation of form "pg. 8, Pedologue Fall 2011 Newsletter – Mid Atlantic Association of Professional Soil Scientists – Stolt and Rabenhorst, 2010. 

In this scientific community, this is often mentioned as desiccation – many prefer a more concrete term – flesh wasting.  At times salt marshes produce toxic compounds able to kill, release nitrogen and most likely effluent leachate that would most likely not meet present regulatory discharge standards.  As we have come to appreciate the value of salt marshes as these negative attributes are usually not often referenced and as no clear explanation of winter kill exists for blue crab points to a bias in our beliefs.  As I said we want oxygen to 'win" and do not highlight the triumphs of sulfur.  When salt marshes become toxic, sulfur is winning – it's just that we just don't talk much about that aspect (See EC #7 posted on Sept 10, 2015, Blue Crab Forum™ Environmental and Conservation thread.  Salt Marsh, A Climate Change Battlefield).

Teodora Bagarinao (Aquatic Toxicology 24 (1992), pg. 21-62 "Sulfate As An Environmental Factor And Toxicant Tolerance And Adaptations In Aquatic Organisms") talks about the volume of marsh and shallow areas as producing 30 million tons of hydrogen sulfide from these aquatic regions noted as the second largest sulfide source on page 24.

"Sediment tests (marsh surface) sulfide is reported as 20 mm to 12 centimeters below the surface but as high in 600 um sulfide in the water column at night with little wind.  Sulfide levels can increase with the presence of a strong thermocline "barrier".  (Hot August nights in CT on occasion produce similar "marsh stink" events.) 
This is a level toxic or stressful to many species, in heat organic deposits continue to purge sulfides in what historically was called "stagnant waters."  One event in Groton, CT in the Poquonnock River conditions were so hot and flows minimal when dense eelgrass and branch (off bottom) oyster aquaculture was blamed on wretched river odors and linked to Scarlet Fever outbreak in the 1880's.  Oyster growers were ordered to remove their brush spat collectors after Sheffield Scientific (Yale) researchers suspected them to be the source of "foul" airs (most likely sulfide).  "Stagnant Water" was blamed for the event and years later and written up in the US Fish Commission Report by Collins.  The Bagarinao report also mentions specific sources as some of the highest sulfide levels have been detected in New Hampshire salt marsh sediments as high as 900-3500 um as reported by Hines et al. (1989).  This level is beyond the tolerance of many estuarine organisms so especially at night when oxygen replenishment is low (no photosynthesis) these waters may become toxic devoid of oxygen (See the 2003 Narragansett Bay Fish Kill produced by RI DEM) and then smell of sulfur.       

In a study of freshwater wetlands, winners or losers is phrased not as in a conflict but "as excess sulfide is produced, it has the potential to chemically transform an ecosystem to a more tolerant community" pg. 8, Schoepher, Valerie The Influence of Sea Water Inundation On Coupled Iron And Sulfur Cycling In A Coastal Fresh Water Wetland (2013).  In other words, the more tolerant community can tolerate more sulfide.  Many fishers and coastal residents might have noticed the smell of sulfur (typically described as rotten eggs) from marshes on hot summer nights and was frequently mentioned in New England during a warm period roughly 1880-1920 I call the Great Heat.  For organisms that needed oxygen in shallow waters there was little great in this for them, this period is known for some of the most notorious fish kills – including the most infamous the Narragansett Bay Fish Kill of 1898 (See Mead 29 Annual Report of the Rhode Island Commissioners of Inland Fisheries – "Investigations Of The Plague Which Destroyed Multitudes Of Fish And Shellfish During The Fall Of 1898") and the immense fish kill of winter flounder in Moriches Bay, New York from July 29th to August 1917.
In high heat and heavy organic matter loading, sulfate reduction occurs (oxygen is now limiting to bacteria that need it) and sulfur reducing bacteria (SRB), able to use sulfate as an oxygen source, simply outcompete oxygen requiring bacteria – in other words they "win" this bacterial war and in the process release toxic sulfides or concentrate sulfide below the immediate surface.  Most salt marsh studies often exclude detailed discussions about sapropel or sulfide formation in them.  Sulfur reduction utilizing sulfate as an oxygen source can also naturally complex heavy metals (especially aluminum) which at times is toxic to both fish and plants.  Salt marshes, therefore, concentrate heavy metals – naturally especially aluminum over periods of time and when sulfuric acid purging occurs release these metals back into the water.  Small striped bass are especially killed by aluminum.

Over periods of time one of the most frequently mentioned reduction pathways is the iron pyrite reduction and oxidation of mono-irons sulfide with gives sapropel its black color. This process is also influenced by the type of organic matter being reduced.  In our area we get a tremendous amount of oak leaves which has a high wax content which helps sulfur reduction by sealing off oxygen (See Cycle of Sapropel).  Sapropels, over time, become sticky with this leaf wax.  It also helps sapropel to take on "jelly" like characteristics.
A walk along a salt marsh small examples of sulfide toxicity can still be seen.  During the Great Heat sulfate reduction below at times caused marsh sections to slump or collapse. Shallow pools often formed called today Pannes – small examples of high heat sulfide formation.  Many Pannes have reduced plant life or no life at all and can climb to over 90oF as sulfides in pool water soar.  Such pannes often have films of white bacteria and contain one of the most tolerant fish species, killifish fundulus – also known as mummichog in our area, which can exist in this extreme low oxygen, high sulfide environment (See Appendix # 1: Sulphide Tolerance and Adaptation in the California Killifish, Fundulus parvipinnis, A Salt Marsh Resident, Bagarinao et al., 1993).
In hot periods such as the 1890's, salt marshes were linked to disease.  In Connecticut and other New England states, salt marshes were often "grid ditched" to lower water tables as a way of eliminating mosquito habitat vectored Malaria.  The last Connecticut Malaria outbreak (5 or more cases) occurred in Connecticut in 1938 and ended as our climate became cooler.  Up until 1912, Connecticut communities were encouraged (and sometimes ordered by State officials) to fill in such habitats as a way of reducing mosquito spread disease.  These "mosquito" ditches cut into Connecticut marshes allowed water tables to drop – allowing oxygen to penetrate the marsh surface as life abounded in these ditches but they were allowed to fill in the 1980's.  As such oxygen containing waters in them reduced as their capacity (flows) were eliminated.  Sulfides in them can rise as oxygen transport was reduced.  As heat increased here after 1974 and accelerated into the 1990's sulfate digestion returned and is mentioned as one of the explanations of recent sudden marsh diebacks in high heat.  These sulfides can kill Spartina, and then allow bare banks to absorb more heat as the peat is "cooked" allowing more bacterial digestion.  The marsh is converted by bacteria to a loose sapropel and then washed away.

Oxidation of marsh organic matter creates sulfuric acid but with tidal action is quickly neutralized by slightly basic seawater.  Sulfides do not form at the immediate marsh surface because oxygen is available from the atmosphere unless sealed by ice or by thick grass "wracks".  A very similar event happens in coastal salt ponds with weak connections to the sea – Ice blocks sunlight and seals atmosphere oxygen sources – ponds and lakes with deep organic deposits over time builds sulfide levels and combines with low oxygen to kill fish.  (Harsh Winter May Spawn Widespread Fish Kills Tom Richardson, March 25, 2015).  Cape Cod has such winter kills in its coastal salt ponds and the State of Massachusetts still issues warnings for them.  Metals are naturally complexed by this sulfur reduction process and can, themselves, be a source of metal and nitrogen/phosphate pollution in high heat – Portnoy (1991) The Cape Cod National Seashore also is looking into this "Marsh" metal pollution aspect.  In a fact sheet titled Herring River titled Frequently – Asked Questions talks about the iron/sulfur cycle when organic matter is reduced and then exposed to oxygen, a section from this fact sheet is quoted below,

"The iron in the pyrite essentially rusts out, liberating the sulfur, which enters the water column as sulfuric acid – this acid lowers the pH of the water values as low as 3.5 pH have been measured following summer rainfalls that washed large amounts of the dried out peat into the water.  This highly acidic water then leaches toxic minerals, (metals) especially aluminum and ferrous iron, out of the clays and organic material in the salt marsh deposits and they wind up in the water column as well." 

Flooding such a marsh will tend to create sulfides, draining it and exposing surface layers to oxygen would allow metals to leach and sulfuric acid to form – Portnoy J. W. 1991.  Summer Oxygen Depletion In A Diked New England Estuary.  Estuaries 14: 122-129.   This in part describes the July 2011 die off Blue Crabs after heavy rains in western CT.  Tannins also are discharged and the source of brown acidic waters.  If accumulations are ripped up by flood waters, a mixture of sulfides, heavy metals can be quickly followed by a sulfuric acid wash.  After tropical storms blue crabbers noticed in some areas of Chesapeake Bay metal crab traps started to dissolve – that is why.   

The potential "pollution" aspect of salt marshes has been known for decades.  Section 22 Wetland Restoration Investigation Leetes Island Salt Marsh, Guilford, CT Dept of the Army Corps of Engineers, March 1994 (CT Office of Long Island Sound programs foreword) details precisely this process.  The report mentions the problems of oxygen reintroduction and the oxygen demands of bacterial reduction:

"When dissolved oxygen levels have been monitored in drained salt marshes low dissolved oxygen levels known as hypoxia have been observed during the summer months especially following rain storms."
Basically, the same process during floods – deep organic layers undergoing sulfur reduction are ripped up and exposed to oxygen – which bacteria cannot "take it" and at the time release acids down streams.
This report (which is a good one on the topic) continues further to introduce the polluting aspect of this salt marsh – when tide gates (or any tide restriction) caused draining – discharges could be a source of metals, nitrogen, phosphate and acids when oxygen levels increased.  On page 2 is found this statement, my comments in (  ):

"Draining cause chemical changes in the soil, which cause the marsh to become a non point source of water pollution. (From the salt marsh – T. Visel) specifically pyrite is unstable when exposed to oxygen through a series of chemical reactions pyrite is converted to sulfuric acid which in turn causes a drastic decrease in soil and creek water pH levels as low as 3 to 4 are not uncommon in drained salt marshes these altered soils are called "acid sulphate soils" Guilford Section 22 Wetlands Restoration Investigations (1994).
This is some of the concern about the trapped sediments collected behind the Conowingo Dam recently large amounts of organic matter once re-exposed to oxygen could purge acids and metals for years (See video clip Violent Soil by Dr. Del Fanning). 

Both acids and metals are toxic components but that just covers the re-exposure of oxygen the shortage of oxygen concentrates phosphate and nitrogen and purges ammonia and sulfides.  (Ammonia levels can become so high it favors different algal species – themselves also negative or harmful termed "HABSs").  Sulfate digestion can occur the marsh surface – studies in Sweden and Europe called it gyttja in peat bogs.  In heat peat bogs underwent underground digestion – by sulfur reducing bacteria and pools of a black liquid formed below under pockets of gas.  This liquid was described as black and has gel like consistency (discussed by Zobell, 1934 "A Comparison of Lead Bismuth and Iron as Detectors of Hydrogen Sulfide Produced by Bacteria").  Sulfate reduction is highest when oxygen is lowest – such as shallow water habitats in summer which obtain leaves from land.  The production of sulfides and sulfuric acids explains why some western CT blue crabbers were concerned with brown waters and dead leaves after heavy rains ended excellent crabbing (Megalops Report #12, August 2, 2011).  They were correct to be concerned.  This rainfall likely released tannins and sulfuric acid.  Waves of blue crabs were then reported leaving the Housatonic River.

The reports around "good" habitat services of salt marshes (which are many) in so many articles conflicts with how some "sediments" are treated and termed today.  I think the Army Corps of Engineers have termed these putrified deposits the best as acidic sulfate soils – but they do not delve into the toxic leachates from them impacting living marine resources.  The terms sedimentation and sediments really do not adequately describe sapropel deposits.  Most definitions mention this sediment as a process broad description from rocks and minerals, as well as plants and animals – The process of weathering or erosion or "unconsolidated deposits and are transported by suspended or deposited by water" (U.S. EPA).  Others term it the weathering of rock, or sand silt and clay (Chesapeake Bay program).  The term sediment I believe is far too broad to fully explain the chemical and biological processes of sapropel.  The Army Corps of Engineers have written about it as their term acidic sulfate soil – is a better one but do not respond to biological implications of it, or the bacterial chelation of metals in it, very few agencies in fact do so today.  The notion that marshes can be a source of "natural nutrient pollution" subject to toxic compound formation and at times help produce natures killing zones is very much in opposition to generally recognized positive public policy attributes (i.e. the high habitat value of salt marshes).  We just don't call it sapropel because it would perhaps signal negative habitat chemistry associations (my feeling) and the bacteria assigned to it.  The definition of sapropel is the decomposition process without oxygen.  It is a marine compost that purges toxins in high heat.  That is contrary to the much perceived public policy of salt marshes as "good" habitats.

Sapropel deposits that contain living plants above or below the surface are part of long habitat succession process that some plants prefer – that is their ecological habitat role so to speak.  Like the terrestrial grasses that follow forest fires – and holds burned soil habitat succession of sapropel that bind loose organics similar to forest soils.  Some of the toxic compounds from sapropel are determined in fact by what organic is matter is being held and reduced.  Oak leaves have tough cellulose structure and sulfur reducing bacteria digest them very slowly.  In areas of oak forests their tannin helps keep the water clear (termed natures clarifier) but in doing so help form the first sapropels.  The very low pH (acidic) leaf and the presence of waxes which are left by bacteria makes sapropel feel greasy or sticky to touch.  It is the wax (also termed paraffin content) that holds your oar or crab net and why in some quiet coves leaves stems turn black and collect by the hundreds of thousands.  Crabbers also noticed that these deposits are those that produce streams of bubbles that is part of the reduction process – other coastal residents on hot August nights report of marsh "sulfur" stinks – the same general process.  Sulfate reduction did cause some researchers to report its salt marsh impacts as the production of hydrogen sulfide gas or methane discharges and at times of high heat slumps of the marsh surface.  Nichols (1920), a century ago, describes this process on some marshes as the digestion of "underground parts" Nichols G.E. 1920 - The Vegetation of Connecticut 111.  The Associations Of Depositing Areas Along The Seacoast – Bulletin of the Torrey Botanical Club 47:11, 548.

In talking about habitat succession Nichols highlights the role of plants in building organic deposits nearly a century ago.
"Plants assist in the building up process in two ways:  first through their mechanical interference with tidal currents, retarding these and causing them to deposit their load of silt, second, through the accumulating of their own dead remains – pg. 543." 

Nichols also provides some clues about the impacts of sealing off oxygen by matts of dead stems and leaves of eelgrass and salt marsh grass also seaweed forms a matt that smothers surface vegetation "setting in rapid decay, not only the aerial plant organs but the underground parts as well, as eventually a depression of some depth may thus arise," pg. 545.

This is the same problem of building structures over muck or organic soils. The slumps in salt marshes, when decomposing vegetation is sealed off from oxygen, are now associated with sulfate reduction of buried organic matter under some of the levees in New Orleans.  Sulfate reduction of long ago buried swamps has been linked as to the cause of a tidal barrier failure in the Katrina New Orleans flooding.  A section of a failed flood wall that was built over high organic deposits (Failure of the I – Wall Flood Protection Structures at New Orleans).  In high heat or over long periods of time salt marsh marshes themselves undergo sulfur digestion, and if sealed from oxygen for long periods, many slump into a cavern of gas – salt pools or pannes.
Keeping the water tables high in salt marshes can slow sulfate reduction but speeds oxidation and release of nitrogen and phosphate compounds, drain the marsh and oxygen can reach those acid sulfate soils below with toxic consequences releasing metals, especially of aluminum which is toxic to fish and acids and can even stunt the growth of Spartina alterniflora but both processes depend upon what bacteria consumes the organic matter, bacteria that need oxygen or those who can use oxygen in sulfur compounds such as sulfate.  Sulfate is not limiting in coastal waters.

Most studies of salt marshes or mud flats do not include discussions about toxic organic deposits or sulfur compounds that can form in them.  They might be mentioned but rarely linked to natural fish and shellfish toxicity.  The case of naturally complexing metals (especially aluminum) and toxicity in salt marshes are not highlighted as a source of these metals.  It is natural for such organic deposits with clays to have high metal fractions.  Aluminum is not usually toxic in seawater as it is slightly alkaline around a pH of 8.  However, salt marshes that obtain oak leaves add acidity and drought lowers the water table and aluminum may leach out at toxic levels.  Aluminum was suspected in the young of the year striped bass failure in the early 1980's.  Brook trout and striped bass are very sensitive to aluminum (EPA 1988, The Guidelines for Deriving Numerical National Water Quality Criteria for the Protection of Aquatic Organisms and Their Uses).

Once acidic sulfate soils (such as those in salt marshes) are exposed to oxidation they can become deadly – they can occur by storms, dredging or tidal restrictions such as dams.  One of the best and complete descriptions of this process is found on the Park Service Cape Cod National Seashore website about the Herring River, Wellfleet, MA, impacted with a dike (tidal restriction) in a fact sheet titled "Herring River Frequently Asked Questions" and mentions that aluminum is toxic to fish – only a few parts per million in the water column.  (This fact sheet provides a clear and read able explanation of the process – one of the best I have found to date).  Sapropel below the surface contains the same sulfate reduction potential and eelgrass a frequent consolidating aggressive grass shares many of the same habitat characteristics that enable it to survive in these deposits, a high leaf silicon content, ability to move oxygen to its roots, and a tolerance to sulfides up to a point.

So how does cold water kill blue crabs?   It doesn't but it is representative of two conditions that can kill blue crabs: (1) ice, which seals off oxygen from bottom waters, and cold water which tends to rip up or erode the bottom after heavy rains; or (2) the rains, themselves, that wash high quantities of organics downstream.  In the final, analysis it is organic matter reduction that may kill the crabs by the chemical processes of organic reduction of sulfide or the metabolism of its toxic by-products into acids.  It is the same factors as Cape Cod salt pond sulfide fish kills only on a much larger scale.  A long cold winter gives sulfide a longer time in which to kill, it could be just as simple as that.  What put sulfide into the soil is perhaps the most important question.

Blue Crabbers have experienced these sulfide bottoms but the smell of dead crabs most likely masked the sulfide odor – the "ticky" crabs mentioned by Van Engle (See Megalops Report #2, April 2015).  It is likely why after tropical rain events Chesapeake blue crabbers experience catch declines when huge rivers of underwater organics blanket bay bottoms and jump start the sulfate reduction process or when reduced organics wash out to form sulfuric acids that dissolved crab pots.

"Bay Grasses" by Josh Bollinger – Feb 13, 2014 has this important account:
The impact of sudden release or deposition of organic matter is devastating to submerged grasses.  This is a section that describes the impact after Agnes.

"I consider Tropical Strom Agnes in 1972, according to Bob Orth a professor at the Virginia Institute is where the problem started.  "It was a knockout punch that had such a dramatic impact on all bay grasses in a very short and narrow period of time" Orth said after Agnes, the grasses were totally gone in many areas.  Once all the grasses are lost, the likelihood of them coming back are slim if you have muddy sediment, he said."
And if the muddy sediment was tested I am certain it would be rich in sulfide and contain some or all sapropel chemical characteristics – T. Visel.  Sudden deposits or current movement of composting organics is also mentioned in the oyster industry historical records.  Once sapropel forms it becomes in heat a toxic habitat for blue crabs.  Testing hibernation areas for sulfide (soil conditions) may provide important clues to when and where blue crabs choose to dig in for the winter – my view, Tim Visel.


Appendix #1
Sulphide Tolerance and Adaptation in the California Killifish, Fundulus parvipinnis, a Salt Marsh Resident
Journal of Fish Biology, Vol. 42, Issue 5
First published: May 1993

By T. Bagarinao & R. D. Vetter


Abstract
Hydrogen sulphide is a toxicant naturally produced in hypoxic marine sediments, hydrocarbon and brine seeps and hydrothermal vents. The California killifish, a salt marsh resident, is remarkably tolerant of sulphide. The 50% lethal concentration is 700 μM total sulphide in 96 h, and 5 mM in 8 h (determined in flow‐through, oxygenated sea water). Killifish exposed to sulphide produce thiosulphate which accumulates in the blood. The cytochrome c oxidase (a major site of toxicity) of the killifish is 50% inhibited by <1 μM sulphide. Killifish liver mitochondria are poisoned by 50–75 μM sulphide but can oxidize 10–20 μM sulphide to thiosulphate. Sulphide causes sulphhaemoglobin formation (and impairment of oxygen transport) at 1–5 mM in vitro and to a small extent at 2 mM in vivo. Killifish blood neither catalyses sulphide oxidation significantly nor binds sulphide at environmental (low) sulphide concentrations. Exposure to 200 μM and 700 μM sulphide over several days causes significant increases in lactate concentrations, indicating shift to anaerobic glycolysis. However, individuals with the most lactate die. In terms of diffusible H2S, the killifish can withstand concentrations two to three orders of magnitude greater than would poison cytochrome c oxidase. The high sulphide tolerance of the killifish, particularly of concentrations typical of salt marshes, can be explained chiefly by mitochondrial sulphide oxidation. Sulphide tolerance and mitochondrial sulphide oxidation in the killifish have a constitutive basis, i.e. do not diminish in fish held in the laboratory in sulphide‐free water for 1–2 months, and are improved by prior acclimation.


Appendix #2
Assessment of the Effects of Bottom Water Temperature & Chemical Conditions, Sediment Temperature, Sedimentary Organic Matter (Type & Amount) on Release of Sulfide and Ammonia from Sediments in Long Island Sound: A Laboratory Study 2004
EPA Long Island Sound Project Descriptions
Final Report Summary
By
Dr. Carmela Cuomo, University of New Haven
Dr. Paul Bartholomew, University of New Haven


Final Report Summary
The goal of this research was to investigate how certain factors in the environment of Western Long Island Sound interact to cause a release of ammonia and/or sulfides, at certain times of the year, from the sediments of WLIS. Factors investigated included: water & sediment temperature, initial water dissolved oxygen (DO) levels, additional of organic matter (plankton), sediment organic content, and the presence or absence of organisms in the sediments. The main findings of the project are as follows: 1. addition of fresh plankton is a significant influence on the release of both ammonia and sulfides from bottom sediments in WLIS. Addition of fresh plankton results in an increase in the release of ammonia from sediments while it results in a general decrease in sulfide release from bottom sediments. 2. The influence of bioturbating organisms on sulfide and ammonia release from WLIS sediments, while not significant (! < 0.10), is present and varies with the other conditions present (i.e., DO, temperature, plankton). 3. The influence of water column DO content on ammonia and sulfide release from sediments is significant but it varies with other factors. 4. The influence of sediment locality on ammonia and sulfide release from sediments, while present, was not significant by itself. However, when taken with plankton, DO, and temperature, locality does exert a significant effect – especially upon sulfide release. Locality was selected as a proxy for organic carbon content. 5. The strongest and most consistent influence on ammonia and sulfide release from sediments under experimental conditions was temperature – both water column and sediment temperature. Sediment temperature consistently tracked water column temperature and ran, on average, 2oC higher than water column temperature. The results of this work demonstrate that temperature, dissolved oxygen, and the addition of plankton, such as happens during the Spring and Fall plankton blooms, all play a significant role in the release of sulfides and ammonia from WLIS sediments. Furthermore, the study suggests that sediment organic content further influences such release.